diff --git a/src/core/dev-server/server.ts b/src/core/dev-server/server.ts
index 7fd90cef37..4f4046548c 100644
--- a/src/core/dev-server/server.ts
+++ b/src/core/dev-server/server.ts
@@ -8,6 +8,7 @@ import { type FSWatcher, watch } from "chokidar";
 import {
   type H3Error,
   type H3Event,
+  appendResponseHeaders,
   createApp,
   createError,
   eventHandler,
@@ -22,15 +23,18 @@ import type {
   Nitro,
   NitroBuildInfo,
   NitroDevServer,
+  NitroRouteRules,
   NitroWorker,
 } from "nitropack/types";
 import { resolve } from "pathe";
 import { debounce } from "perfect-debounce";
 import { servePlaceholder } from "serve-placeholder";
 import serveStatic from "serve-static";
-import { joinURL } from "ufo";
+import { joinURL, withoutBase } from "ufo";
 import defaultErrorHandler from "./error";
 import { createVFSHandler } from "./vfs";
+import { createRouter as createRadixRouter, toRouteMatcher } from "radix3";
+import defu from "defu";
 
 function initWorker(filename: string): Promise<NitroWorker> | undefined {
   if (!existsSync(filename)) {
@@ -166,6 +170,20 @@ export function createDevServer(nitro: Nitro): NitroDevServer {
   // Debugging endpoint to view vfs
   app.use("/_vfs", createVFSHandler(nitro));
 
+  // Apply headers based on routeRules. In cases where the dev server is being
+  // used, these would otherwise fail to be applied to public assets.
+  const routeRulesMatcher = toRouteMatcher(
+    createRadixRouter({ routes: nitro.options.routeRules })
+  );
+  app.use("/", eventHandler((event) => {
+    const baseUrl = nitro.options.runtimeConfig.app.baseURL;
+    const normPath = withoutBase(event.path.split("?")[0], baseUrl);
+    const rules: NitroRouteRules = defu({}, ...routeRulesMatcher.matchAll(normPath).reverse());
+    if (rules.headers) {
+      appendResponseHeaders(event, rules.headers);
+    }
+  }));
+
   // Serve asset dirs
   for (const asset of nitro.options.publicAssets) {
     const url = joinURL(